Functional Reorganization of the Mesial Frontal Premotor Cortex in Patients With Supplementary Motor Area Seizures

Neurosurgery 92:186–194, 2023

Direct cortical stimulation of the mesial frontal premotor cortex, including the supplementary motor area (SMA), is challenging in humans. Limited access to these brain regions impedes understanding of human premotor cortex functional organization and somatotopy.

OBJECTIVE: To test whether seizure onset within the SMA was associated with functional remapping of mesial frontal premotor areas in a cohort of patients with epilepsy who underwent awake brain mapping after implantation of interhemispheric subdural electrodes.

METHODS: Stimulation trials from 646 interhemispheric subdural electrodes were analyzed and compared between patients who had seizure onset in the SMA (n = 13) vs patients who had seizure onset outside of the SMA (n = 12). 1:1 matching with replacement between SMA and non-SMA data sets was used to ensure similar spatial distribution of electrodes. Centroids and 95% confidence regions were computed for clustered head, trunk, upper extremity, lower extremity, and vision responses. A generalized linear mixedeffects model was used to test for significant differences in the resulting functional maps. Clinical, radiographic, and histopathologic data were reviewed.

RESULTS: After analyzing direct cortical stimulation trials from interhemispheric electrodes, we found significant displacement of the head and trunk responses in SMA compared with non-SMA patients (P < .01 for both). These differences remained significant after accounting for structural lesions, preexisting motor deficits, and seizure outcome.

CONCLUSION: The somatotopy of the mesial frontal premotor regions is significantly altered in patients who have SMA-onset seizures compared with patients who have seizure onset outside of the SMA, suggesting that functional remapping can occur in these brain regions.

Mapping and anatomo-surgical techniques for SMA-cingulum-corpus callosum gliomas

Acta Neurochirurgica (2021) 163:1239–1246

Awake brain mapping paradigms are variable, particularly in SMA, and not personalised to each patient. In addition, subpial resections do not offer full protection to vascular injury, as the pia can be easily violated.

Methods Mapping paradigms developed by a multidisciplinary brain mapping team. During resection, a combined subpial/ interhemispheric approach allowed early identification and arterial skeletonization. Precise anatomo-surgical dissection of the affected cingulum and corpus callosum was achieved.

Conclusions In SMA-cingulum-CC tumours, a combined subpial/interhemispheric approach reduces risk of vascular injury allowing precise anatomo-surgical dissections. Knowledge of cognitive functions of affected parcels is likely to offer best outcomes.

Long-term surgical results of supplementary motor area epilepsy surgery

J Neurosurg 127:1153–1159, 2017

Supplementary motor area (SMA) epilepsy is a well-known clinical condition; however, long-term surgical outcome reports are scarce and correspond to small series or isolated case reports. The aim of this study is to present the surgical results of SMA epilepsy patients treated at 2 reference centers in Mexico City.

METHODS For this retrospective descriptive study (1999–2014), 52 patients underwent lesionectomy and/or corticectomy of the SMA that was guided by electrocorticography (ECoG). The clinical, neurophysiological, neuroimaging, and pathological findings are described. The Engel scale was used to classify surgical outcome. Descriptive statistics, Student t-test, and Friedman, Kruskal-Wallis, and chi-square tests were used.

RESULTS Of these 52 patients, the mean age at epilepsy onset was 26.3 years, and the mean preoperative seizure frequency was 14 seizures per month. Etiologies included low-grade tumors in 28 (53.8%) patients, cortical dysplasia in 17 (32.7%) patients, and cavernomas in 7 (13.5%) patients. At a mean follow-up of 5.7 years (range 1–10 years), 32 patients (61%) were classified as Engel Class I, 16 patients (31%) were classified as Engel Class II, and 4 (8%) patients were classified as Engel Class III. Overall seizure reduction was significant (p = 0.001). The absence of early postsurgical seizures and lesional etiology were associated with the outcome of Engel Class I (p = 0.05). Twenty-six (50%) patients had complications in the immediate postoperative period, all of which resolved completely with no residual neurological deficits.

CONCLUSIONS Surgery for SMA epilepsy guided by ECoG using a multidisciplinary and multimodality approach is a safe, feasible procedure that shows good seizure control, moderate morbidity, and no mortality.

Risk factor analysis of the development of new neurological deficits following supplementary motor area resection

Supplementary motor area

J Neurosurg 119:7–14, 2013

Supplementary motor area (SMA) resection often induces postoperative contralateral hemiparesis or speech disturbance. This study was performed to assess the neurological impairments that often follow SMA resection and to assess the risk factors associated with these postoperative deficits.

Methods. The records for patients who had undergone SMA resection for pharmacologically intractable epilepsy between 1994 and 2010 were gleaned from an epilepsy surgery database and retrospectively reviewed in this study.

Results. Forty-three patients with pharmacologically intractable epilepsy underwent SMA resection with intraoperative cortical stimulation and mapping while under awake anesthesia. The mean patient age was 31.7 years (range 15–63 years), and the mean duration and frequency of seizures were 10.4 years (range 0.1–30 years) and 14.6 per month (range 0.1–150 per month), respectively. Pathological examination of the brain revealed cortical dysplasia in 18 patients (41.9%), tumors in 16 patients (37.2%), and other lesions in 9 patients (20.9%). The mean duration of the follow-up period was 84.0 months (range 24–169 months). After SMA resection, 23 patients (53.5%) experienced neurological deficits. Three patients (7.0%) experienced permanent deficits, and 20 (46.5%) experienced symptoms that were transient. All permanent deficits involved contralateral weakness, whereas the transient symptoms patients experienced were varied, including contralateral weaknesses in 15, apraxia in 1, sensory disturbances in 1, and dysphasia in 6. Thirteen patients recovered completely within 1 month. Univariate analysis revealed that resection of the SMA proper, a shorter lifetime seizure history (< 10 years), and resection of the cingulate gyrus in addition to the SMA were associated with the development of neurological deficits (p = 0.078, 0.069, and 0.023, respectively). Cingulate gyrus resection was the only risk factor identified on multivariate analysis (p = 0.027, OR 6.530, 95% CI 1.234–34.562).

Conclusions. Resection of the cingulate gyrus in addition to the SMA was significantly associated with the development of postoperative neurological impairment.

Agraphia after awake surgery for brain tumor: new insights into the anatomo-functional network of writing

Surgical Neurology. Volume 72, Issue 3, Pages 223-241 (September 2009)

Background

Controversy still exists about neural basis underlying writing and its relation with the sites subserving oral language. Our objective is to study functional areas involved in writing network, based on the observations of different postoperative writing disorders in a population of patients without preoperative agraphia.

Methods

We analyzed the postoperative agraphia profiles in 15 patients who underwent surgery for cerebral LGGs in functional language areas, using electrical mapping under local anesthesia. These profiles were then correlated to the sites of the lesions, shown by preoperative cerebral imaging.

Results

Our findings showed that (1) spoken language and writing functions could be dissociated, and that (2) writing is subserved, at least partially, by a network of 5 areas located in the dominant hemisphere for language: the superior parietal region, the supramarginalis gyrus, the second and third frontal convolutions, the supplementary motor area, and the insula. Each of these areas seems to have a different role in writing, which will be detailed in this article. However, among the patients, only those with lesions of the supplementary motor area did not recover from agraphia in the postoperative period (in 50% of cases).

Conclusions

On the basis of these results, and in the light of the recent literature, we discuss the relevance of each area in this anatomo-functional network as well as the clinical implications of such better knowledge of the neural basis of writing, especially for brain surgery and functional rehabilitation.